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      Enhanced Nitrous Oxide Production in Denitrifying Dechloromonas aromatica Strain RCB Under Salt or Alkaline Stress Conditions

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          Abstract

          Salinity and pH have direct and indirect impacts on the growth and metabolic activities of microorganisms. In this study, the effects of salt and alkaline stresses on the kinetic balance between nitrous oxide (N 2O) production and consumption in the denitrification pathway of Dechloromonas aromatica strain RCB were examined. N 2O accumulated transiently only in insignificant amounts at low salinity (≤0.5% NaCl) and circumneutral pH (7.0 and 7.5). As compared to these control conditions, incubation at 0.7% salinity resulted in substantially longer lag phase and slower growth rate, along with the increase in the amounts of transiently accumulated N 2O (15.8 ± 2.8 μmoles N 2O-N/vessel). Incubation at pH 8.0 severely inhibited growth and resulted in permanent accumulation of 29.9 ± 1.3 μmoles N 2O-N/vessel from reduction of 151 ± 20 μmoles NO 3 /vessel. Monitoring of temporal changes in nirS 1, nirS 2, and nosZ transcription suggested that the nosZ/( nirS 1+ nirS 2) ratios were indicative of whether N 2O was produced or consumed at the time points where measurements were taken. The salt and alkaline stresses altered the N 2O consumption kinetics of the resting D. aromatica cells with expressed nitrous oxide reductases. The N 2O consumption rates of the cells subjected to the salt and alkaline stress conditions were significantly reduced from 0.84 ± 0.007 μmoles min −1 mg protein −1 of the control to 0.27 ± 0.02 μmoles min −1 mg protein −1 and 0.31 ± 0.03 μmoles min −1 mg protein −1, respectively, when the initial dissolved N 2O concentration was 0.1 mM. As the rates of N 2O production from NO 2 reduction was not significantly affected by the stresses (0.45–0.55 μmoles min −1 mg protein −1), the N 2O consumption rate was lower than the N 2O production rate at the stress conditions, but not at the control condition. These results clearly indicate that the altered kinetics of expressed nitrous oxide reductase and the resultant disruption of kinetic balance between N 2O production and consumption was another cause of enhanced N 2O emission observed under the salt and alkaline stress conditions. These findings suggest that canonical denitrifiers may become a significant N 2O source when faced with abrupt environmental changes.

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          Cell biology and molecular basis of denitrification.

          W Zumft (1997)
          Denitrification is a distinct means of energy conservation, making use of N oxides as terminal electron acceptors for cellular bioenergetics under anaerobic, microaerophilic, and occasionally aerobic conditions. The process is an essential branch of the global N cycle, reversing dinitrogen fixation, and is associated with chemolithotrophic, phototrophic, diazotrophic, or organotrophic metabolism but generally not with obligately anaerobic life. Discovered more than a century ago and believed to be exclusively a bacterial trait, denitrification has now been found in halophilic and hyperthermophilic archaea and in the mitochondria of fungi, raising evolutionarily intriguing vistas. Important advances in the biochemical characterization of denitrification and the underlying genetics have been achieved with Pseudomonas stutzeri, Pseudomonas aeruginosa, Paracoccus denitrificans, Ralstonia eutropha, and Rhodobacter sphaeroides. Pseudomonads represent one of the largest assemblies of the denitrifying bacteria within a single genus, favoring their use as model organisms. Around 50 genes are required within a single bacterium to encode the core structures of the denitrification apparatus. Much of the denitrification process of gram-negative bacteria has been found confined to the periplasm, whereas the topology and enzymology of the gram-positive bacteria are less well established. The activation and enzymatic transformation of N oxides is based on the redox chemistry of Fe, Cu, and Mo. Biochemical breakthroughs have included the X-ray structures of the two types of respiratory nitrite reductases and the isolation of the novel enzymes nitric oxide reductase and nitrous oxide reductase, as well as their structural characterization by indirect spectroscopic means. This revealed unexpected relationships among denitrification enzymes and respiratory oxygen reductases. Denitrification is intimately related to fundamental cellular processes that include primary and secondary transport, protein translocation, cytochrome c biogenesis, anaerobic gene regulation, metalloprotein assembly, and the biosynthesis of the cofactors molybdopterin and heme D1. An important class of regulators for the anaerobic expression of the denitrification apparatus are transcription factors of the greater FNR family. Nitrate and nitric oxide, in addition to being respiratory substrates, have been identified as signaling molecules for the induction of distinct N oxide-metabolizing enzymes.
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            Non-CO2 greenhouse gases and climate change.

            Earth's climate is warming as a result of anthropogenic emissions of greenhouse gases, particularly carbon dioxide (CO(2)) from fossil fuel combustion. Anthropogenic emissions of non-CO(2) greenhouse gases, such as methane, nitrous oxide and ozone-depleting substances (largely from sources other than fossil fuels), also contribute significantly to warming. Some non-CO(2) greenhouse gases have much shorter lifetimes than CO(2), so reducing their emissions offers an additional opportunity to lessen future climate change. Although it is clear that sustainably reducing the warming influence of greenhouse gases will be possible only with substantial cuts in emissions of CO(2), reducing non-CO(2) greenhouse gas emissions would be a relatively quick way of contributing to this goal.
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              454 pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants.

              Activated sludge (AS) contains highly complex microbial communities. In this study, PCR-based 454 pyrosequencing was applied to investigate the bacterial communities of AS samples from 14 sewage treatment plants of Asia (mainland China, Hong Kong, and Singapore), and North America (Canada and the United States). A total of 259 K effective sequences of 16S rRNA gene V4 region were obtained from these AS samples. These sequences revealed huge amount of operational taxonomic units (OTUs) in AS, that is, 1183-3567 OTUs in a sludge sample, at 3% cutoff level and sequencing depth of 16,489 sequences. Clear geographical differences among the AS samples from Asia and North America were revealed by (1) cluster analyses based on abundances of OTUs or the genus/family/order assigned by Ribosomal Database Project (RDP) and (2) the principal coordinate analyses based on OTUs abundances, RDP taxa abundances and UniFrac of OTUs and their distances. In addition to certain unique bacterial populations in each AS sample, some genera were dominant, and core populations shared by multiple samples, including two commonly reported genera of Zoogloea and Dechloromonas, three genera not frequently reported (i.e., Prosthecobacter, Caldilinea and Tricoccus) and three genera not well described so far (i.e., Gp4 and Gp6 in Acidobacteria and Subdivision3 genera incertae sedis of Verrucomicrobia). Pyrosequencing analyses of multiple AS samples in this study also revealed the minority populations that are hard to be explored by traditional molecular methods and showed that a large proportion of sequences could not be assigned to taxonomic affiliations even at the phylum/class levels.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                05 June 2019
                2019
                : 10
                : 1203
                Affiliations
                [1] 1Department of Civil and Environmental Engineering, Korea Advanced Institute of Science and Technology , Daejeon, South Korea
                [2] 2Department of Biological Sciences, Virginia Institute of Marine Science, College of William and Mary , Gloucester Point, VA, United States
                Author notes

                Edited by: Haike Antelmann, Freie Universität Berlin, Germany

                Reviewed by: Koki Maeda, Japan International Research Center for Agricultural Sciences, Japan; Lars Reier Bakken, Norwegian University of Life Sciences, Norway; Bing-Jie Ni, The University of Queensland, Australia

                *Correspondence: Sukhwan Yoon, syoon80@ 123456kaist.ac.kr

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.01203
                6593283
                a130ca6f-7a1f-4d48-b925-c3e4e3807a2f
                Copyright © 2019 Han, Song, Song and Yoon.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 March 2019
                : 13 May 2019
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 60, Pages: 11, Words: 0
                Funding
                Funded by: Ministry of the Environment 10.13039/501100006120
                Award ID: 2017002420002
                Funded by: National Research Foundation of Korea 10.13039/501100003725
                Award ID: 2018H1D3A2063734
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                denitrification,nitrous oxide,salt stress,alkaline stress,rt-qpcr,kinetics
                Microbiology & Virology
                denitrification, nitrous oxide, salt stress, alkaline stress, rt-qpcr, kinetics

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